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The Universal Tree of Life: an Update

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The Universal Tree of Life: an Update REVIEW published: 21 July 2015 doi: 10.3389/fmicb.2015.00717 The universal tree of life: an update Patrick Forterre 1,2* 1 Unité de Biologie Moléculaire du Gène chez les Extrêmophiles, Département de Microbiologie, Institut Pasteur, Paris, France, 2 Institut de Biologie Intégrative de la cellule, Université Paris-Saclay, Paris, France Biologists used to draw schematic “universal” trees of life as metaphors illustrating the history of life. It is indeed a priori possible to construct an organismal tree connecting the three major domains of ribosome encoding organisms: Archaea, Bacteria and Eukarya, since they originated by cell division from LUCA. Several universal trees based on ribosomal RNA sequence comparisons proposed at the end of the last century are still widely used, although some of their main features have been challenged by subsequent analyses. Several authors have proposed to replace the traditional universal tree with a ring of life, whereas others have proposed more recently to include viruses as new domains. These proposals are misleading, suggesting that endosymbiosis can modify the shape of a tree or that viruses originated from the last universal common ancestor (LUCA). Edited by: I propose here an updated version of Woese’s universal tree that includes several rootings Mechthild Pohlschroder, University of Pennsylvania, USA for each domain and internal branching within domains that are supported by recent Reviewed by: phylogenomic analyses of domain specific proteins. The tree is rooted between Bacteria Dong-Woo Lee, and Arkarya, a new name proposed for the clade grouping Archaea and Eukarya. A Kyungpook National University, South Korea consensus version, in which each of the three domains is unrooted, and a version in which Reinhard Rachel, eukaryotes emerged within archaea are also presented. This last scenario assumes the University of Regensburg, transformation of a modern domain into another, a controversial evolutionary pathway. Germany David Penny, Viruses are not indicated in these trees but are intrinsically present because they infect Massey University, New Zealand the tree from its roots to its leaves. Finally, I present a detailed tree of the domain *Correspondence: Archaea, proposing the sub-phylum neo-Euryarchaeota for the monophyletic group of Patrick Forterre, Unité de Biologie Moléculaire du euryarchaeota containing DNA gyrase. These trees, that will be easily updated as new Gène chez les Extrêmophiles, data become available, could be useful to discuss controversial scenarios regarding early Département de Microbiologie, life evolution. Institut Pasteur, 25 Rue du Docteur Roux, Paris 75015, France Keywords: archaea, bacteria, eukarya, LUCA, universal tree, evolution [email protected] Introduction Specialty section: This article was submitted to The editors of research topic on “archaeal cell envelopes and surface structures” gave me the Microbial Physiology and Metabolism, challenging task of drawing an updated version of the universal tree of life. This is a daunting a section of the journal Frontiers in Microbiology task indeed, given that the concept of a universal “tree” is disputed by some scientists, who have suggested replacing trees with networks, and that major features of the tree are still controversial Received: 05 January 2015 Accepted: 29 June 2015 (Gribaldo et al., 2010; Forterre, 2012). Thus, it will be difficult to draw a consensus tree welcomed Published: 21 July 2015 by all scientists in the field. In this paper, I thus try to propose updated versions of the universal tree that include as many features as possible validated by robust phylogenetic analyses and/or Citation: Forterre P (2015) The universal tree comparative molecular biology and biochemistry. I will draw a “universal tree” limited to ribosome- of life: an update. encoding organisms (Raoult and Forterre, 2008) that diverged from the last universal common Front. Microbiol. 6:717. ancestor (LUCA). Viruses (capsid encoding organisms) are polyphyletic, therefore their evolution doi: 10.3389/fmicb.2015.00717 can be neither illustrated by a single tree nor included in the universal tree as additional domains Frontiers in Microbiology | www.frontiersin.org 1 July 2015 | Volume 6 | Article 717 Forterre The universal tree of life (Forterre et al., 2014a). However, this should not be viewed as some major lineages identified in the past decade, such as the neglecting the role of viruses in biological evolution because “the Thaumarchaeota, which are now recognized as one of the three tree of life is infected by viruses from the root to the leaves”(Forterre major archaeal phyla (Brochier-Armanet et al., 2008a; Spang et al., et al., 2014a). The universal tree of ribosome-encoding organisms 2010, 2015). contains cellular organisms that, unlike viruses, reproduce via cell cycles that imply the formation of new cells from the division of Problems with Textbook Trees mother cells. This implies a fascinating continuity in the heredity of the cell membrane from LUCA to modern members of the three The universal trees of the 1990s based on rDNA that are still widely domains. A robust universal tree is critical to make sense of the used in textbooks, reviews and seminars provide a misleading evolution of the several types of lipids, cell envelopes and surface view of the history of organisms. For instance, they all depict the structures that originated and evolved on top of this continuity. division of Eukarya between a crown including Plants, Metazoa, Fungi, and several lineages of protists, and several basal long The Textbook Trees branches leading to various other unicellular eukaryotes, of which the most basal are protists lacking mitochondria (formerly called Several popular drawings of the universal tree of life are Archaezoa). This topology of the eukaryotic tree was very popular widespread in the scientific literature and textbooks. These in the 1990s but is the result of a long branch attraction artifact. include the radial rRNA tree of Pace (1997), the tree of Stetter At the beginning of this century, it was acknowledged that all (1996) rooted in a hyperthermophilic LUCA and the most famous major eukaryotic divisions should be somewhere in the crown tree, which was published by Woese et al. (1990) to support their (Embley and Hirt, 1998; Keeling and McFadden, 1998; Philippe proposal to change the name “Archaebacteria” to Archaea and to and Adoutte, 1998; Gribaldo and Philippe, 2002). define the Domain as the highest taxonomic level (Woese et al., Another problem still present in many textbook trees is the 1990; Sapp, 2009). All these trees are based on ribosomal DNA position of hyperthermophiles. All rDNA trees of the 1990s (rDNA) sequence comparisons and are rooted between Bacteria were rooted within hyperthermophilic archaea and bacteria and a common ancestor of Archaea and Eukarya, a rooting (Woese et al., 1990; Stetter, 1996; Pace, 1997). In particular, that was first suggested by phylogenetic analyses of paralogous the hyperthermophilic bacteria of the genera Thermotoga and proteins (Iwabe et al., 1989; Gogarten et al., 1989). Aquifex were the two most basal bacterial lineages in all these The rDNA trees are still widely used despite their age (from 17 trees. This explains why these bacteria are still often labeled to 25 years old) because scientists need metaphors to represent as “deep-branching bacteria” (Braakman and Smith, 2014). the history of living organisms (despite all criticisms to the tree However, the analysis of ribosomal RNA sequences at slowly concept itself) and because few new trees have been proposed in evolving nucleotide positions (Brochier and Philippe, 2002) and the past two decades that are accepted by most biologists. Doolittle phylogenetic analyses based on protein sequences do not support (2000) published a widely popularized tree in which the bases of the deep branching of Thermotoga and Aquifex in the bacterial the three domains are mixed by widespread lateral gene transfer tree (Boussau et al., 2008b; Zhaxybayeva et al., 2009). The exact (LGT). However, studies on archaeal phylogeny and more recently position of these hyperthermophilic bacteria currently remains in Bacteria and Eukarya, as well as comparative genomic analyses, controversial, because of the unusual extent of LGT that occurred have shown that the history of organisms (not to be confused between these bacteria and some other bacterial groups (Boussau with the history of genes) can be inferred from a core of highly et al., 2008b; Zhaxybayeva et al., 2009; Eveleigh et al., 2013). conserved genes (Brochier et al., 2005a; Gribaldo and Brochier, The clustering of hyperthermophiles around the root and their 2009; Puigbò et al., 2013; He et al., 2014; Ramulu et al., 2014; “short branches” have been widely cited as support for the idea Raymann et al., 2014; Petitjean et al., 2015). of a hot LUCA and a hot origin of life (Stetter, 1996), although Comparative genomics has confirmed the existence of three the phenotype of an organism at the tip of a branch does not versions (sensu Woese) of all universally conserved proteins, necessarily reflect that of its ancestor at the base. However, early validating the three domains concept at the genomic level reports noted that both features could be explained by the very and opening the way to protein based universal trees (Olsen high GC content of the ribosomal RNA of hyperthermophiles and Woese, 1997). A fairly popular radial tree based on a that limits the sequence space available
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